Seasonal Dynamics and Damage of Halyomorpha halys in Italian Vineyards.

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is an invasive polyphagous pest often observed in vineyards. In Europe, a gap needs to be filled in the knowledge on H. halys seasonal dynamics and damage on grapes. With this study, we described the seasonal dynamics of H. halys and its distribution in multi-cultivar vineyards, and we evaluated the damage on grape clusters induced by different pest densities. In vineyards, the seasonal occurrence of H. halys varied across time and grape cultivars, and the pest was more abundant on Cabernet Franc, Merlot and, to a lesser extent, Pinot gris. Moreover, higher densities of H. halys were found on red berry cultivars than on white ones, and on cultivars ripening late in the season. An edge effect was also detected in pest distribution within vineyards, with more stink bugs observed in the borders. In the study on pest infestation density, H. halys caused damage on berries, showing differences in susceptibility among different cultivars and with regard to the time of infestation (i.e., plant phenological stages). Halyomorpha halys infestation induced an increase in Botrytis cinerea and sour rot incidence, which probably represents the main issue related to the impact of brown marmorated stink bug on grapevine.

Evaluating the Impact of Two Generalist Predators on the Leafhopper Erasmoneura vulnerata Population Density.

Outbreaks of the Nearctic leafhopper Erasmoneura vulnerata represent a threat to vinegrowers in Southern Europe, in particular in North-eastern Italy. The pest outbreaks are frequent in organic vineyards because insecticides labeled for organic viticulture show limited effectiveness towards leafhoppers. On the other hand, the naturally occurring predators and parasitoids of E. vulnerata in vineyards are often not able to keep leafhopper densities at acceptable levels for vine-growers. In this study, we evaluated the potential of two generalist, commercially available predators, Chrysoperla carnea and Orius majusculus, in suppressing E. vulnerata. Laboratory and semi-field experiments were carried out to evaluate both species' predation capacity on E. vulnerata nymphs. The experiments were conducted on grapevine leaves inside Petri dishes (laboratory) and on potted and caged grapevines (semi-field); in both experiments, the leaves or potted plants were infested with E. vulnerata nymphs prior to predator releases. Both predator species exhibited a remarkable voracity and significantly reduced leafhopper densities in laboratory and semi-field experiments. Therefore, field studies were carried out over two growing seasons in two vineyards. We released 4 O. majusculus adults and 30 C. carnea larvae per m2 of canopy. Predator releases in vineyards reduced leafhopper densities by about 30% compared to the control plots. Results obtained in this study showed that the two predators have a potential to suppress the pest density, but more research is required to define appropriate predator-prey release ratios and release timing. Studies on intraguild interactions and competition with naturally occurring predators are also suggested.

The Control of the American Leafhopper Erasmoneura vulnerata (Fitch) in European Vineyards: Impact of Synthetic and Natural Insecticides.

The American leafhopper Erasmoneura vulnerata, detected in Europe in the early 2000s, has recently become a pest in North-Italian vineyards. Infestations were recorded in organic and conventional vineyards despite the application of insecticides targeting other pests. Erasmoneura vulnerata completes three generations per year, and the second generation is frequently associated with large populations. The selection of appropriate active ingredients and the timing of their application is crucial for effective pest control. Field trials were carried out in Northeastern Italy, using a randomized design, to evaluate the impact of insecticides applied against other grapevine leafhoppers on E. vulnerata populations. The beginning of the second generation was selected as the best time for insecticide application. For natural products, two applications were planned. Among the selected insecticides, the most effective were acetamiprid, flupyradifurone and lambda-cyhalothrin. Regarding natural products, the most effective was kaolin which could represent an alternative to pyrethrins in organic vineyards. The identification of pest threshold levels and the evaluation of side effects of the most effective insecticides on key natural enemies occurring in vineyards are required.

Correction: Duso C.; et al. Colonization Patterns, Phenology and Seasonal Abundance of the Nearctic Leafhopper Erasmoneura vulnerata (Fitch), a New Pest in European Vineyards. Insects 2020, 11, 731.

It has recently come to our attention that there were some mistakes in legends and figures reported in our study [...].

Colonization Patterns, Phenology and Seasonal Abundance of the Nearctic Leafhopper Erasmoneura vulnerata (Fitch), a New Pest in European Vineyards.

The Nearctic leafhopper Erasmoneura vulnerata (Fitch), detected in Europe for the first time (north-eastern Italy) in 2004, has remained a minor pest of grapevine for more than 10 years. The first outbreaks of E. vulnerata were reported in 2016 in commercial vineyards located in north-eastern Italy. High population densities and severe leaf symptoms (i.e., leaf discoloration and fall) were observed in late summer despite the application of insecticides. Investigations were carried out from 2017 to 2019 in 10 vineyards located in Veneto region (Vicenza and Verona provinces) to shed light on the seasonal abundance of E. vulnerata on different Vitis vinifera cultivars. Pest phenology was studied in six vineyards where the impact of insecticides was minimal. Erasmoneura vulnerata completed three generations in each of the growing seasons. Vineyard colonization by overwintered adults showed a clear edge effect, suggesting the influence of overwintering sites (e.g., rural buildings and hedgerows) in vineyard margins. The impact of natural enemies on pest populations appeared to be limited and mostly related to egg parasitoids. Organic vineyards were more heavily infested by E. vulnerata compared to conventional vineyards, likely due to the minimal efficacy of natural insecticides typically used in the former farms.

Lethal and sub-lethal effects of low-temperature exposures on Halyomorpha halys (Hemiptera: Pentatomidae) adults before and after overwintering.

Cold winter temperatures can influence insects' survival in temperate zones. Brown marmorated stink bug, Halyomorpha halys (Stål) overwinters as adults in natural and human-made structures. In this study, we characterized low temperature mortality rates of H. halys adults that were either entering (ENA) or exiting (EXA) overwintering microhabitats. We considered the effect of different duration of cold exposure on mortality. We determined the impact of insect nutritional status and weight on cold tolerance. We additionally evaluated the effects of cold exposure on H. halys adult longevity and fecundity. Mortality of ENA and EXA adults was determined for 6 h and 2 h periods at - 2.5 °C and 2.5 °C respectively. EXA adults displayed higher mortality rates compared to ENA individuals at the low-temperature regimes. Halyomorpha halys adult survival rate was higher when their nutrient index (EXA individuals only) and weight were high. Low-temperature exposure increased longevity, but reduced fecundity of ENA females. The data further highlight how extreme spring frost events can result in significantly increased mortality levels of H. halys adults.

An Insight into the Role of Trissolcus mitsukurii as Biological Control Agent of Halyomorpha halys in Northeastern Italy.

Sustainable strategies such as classical or augmentative biological control are currently being evaluated for the long-term management of the alien invasive pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). A three-year study carried out in northeastern Italy was performed to investigate the distribution and field performance of the H. halys egg parasitoid Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae), in comparison with other parasitoid species. In the study area, adventive populations of T. mitsukurii were present since 2016, representing the earliest detection of this species in Europe. Trissolcus mitsukurii was the most abundant parasitoid and showed a higher "parasitoid impact" (i.e., number of parasitized eggs over the total number of field-collected eggs) compared to the other species, i.e., Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae), Trissolcus basalis (Wollaston) and Trissolcus kozlovi Rjachovskij (Hymenoptera: Scelionidae). The hyperparasitoid Acroclisoides sinicus (Huang and Liao) (Hymenoptera: Pteromalidae) was also recorded. Phylogenetic analysis of T. mitsukurii population distinguished two clades, one covering samples from Italy, Japan and China, the other from South Korea. The present study provides promising results for the biological control of a pest that is having a dramatic impact on a wide range of crops worldwide.

Side Effects of Kaolin and Bunch-Zone Leaf Removal on Predatory Mite Populations (Acari: Phytoseiidae) Occurring in Vineyards.

The effects of kaolin and bunch-zone leaf removal on populations of predatory mites Kampimodromus aberrans (Oudemans) and Typhlodromus pyri Scheuten were assessed in the context of four trials (2015-2016) carried out against Lobesia botrana (Denis and Schiffermüller) (Lepidoptera: Tortricidae) in vineyards located in north-eastern Italy. Laboratory experiments were performed to evaluate the effects of kaolin on the survival and fecundity of K. aberrans and T. pyri populations originating from the same grape-growing area. In field trials, kaolin caused a gradual decrease in population density levels of both phytoseiid species (with the maximum reduction ranging from 49 to 91%) with a complete population recovery in the next spring. In laboratory experiments, kaolin was moderately harmful to both species, reducing their fecundity significantly (around 60%). Bunch-zone leaf removal determined lower phytoseiid populations in all trials, but this effect was significant only for K. aberrans in one of them. A limited use of kaolin and the adoption of bunch-zone leaf removal did not irreversibly affect phytoseiid populations in vineyards and thus can be considered compatible with IPM strategies.

A Fundamental Step in IPM on Grapevine: Evaluating the Side Effects of Pesticides on Predatory Mites.

Knowledge on side effects of pesticides on non-target beneficial arthropods is a key point in Integrated Pest Management (IPM). Here we present the results of four experiments conducted in vineyards where the effects of chlorpyrifos, thiamethoxam, indoxacarb, flufenoxuron, and tebufenozide were evaluated on the generalist predatory mites Typhlodromus pyri Scheuten and Amblyseius andersoni (Chant), key biocontrol agents of herbivorous mites on grapevines. Results show that indoxacarb and tebufenozide had a low impact on the predatory mites considered here, while a significant impact was observed for chlorpyrifos, flufenoxuron, and thiamethoxam. The information obtained here should be considered in the design of IPM strategies on grapevine.

The impact of insecticides applied in apple orchards on the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae).

Kampimodromus aberrans is an effective predatory mite in fruit orchards. The side-effects of insecticides on this species have been little studied. Field and laboratory experiments were conducted to evaluate the effects of insecticides on K. aberrans. Field experiments showed the detrimental effects of etofenprox, tau-fluvalinate and spinosad on predatory mites. Spider mite (Panonychus ulmi) populations reached higher densities on plots treated with etofenprox and tau-fluvalinate than in the other treatments. Single or multiple applications of neonicotinoids caused no detrimental effects on predatory mites. In the laboratory, spinosad and tau-fluvalinate caused 100 % mortality. Etofenprox caused a significant mortality and reduced fecundity. The remaining insecticides did not affect female survival except for imidacloprid. Thiamethoxam, clothianidin, thiacloprid, chlorpyrifos, lufenuron and methoxyfenozide were associated with a significant reduction in fecundity. No effect on fecundity was found for indoxacarb or acetamiprid. Escape rate of K. aberrans in laboratory was relatively high for etofenprox and spinosad, and to a lesser extent thiacloprid. The use of etofenprox, tau-fluvalinate and spinosad was detrimental for K. aberrans and the first two insecticides induced spider mite population increases. The remaining insecticides caused no negative effects on predatory mites in field trials. Some of them (reduced fecundity and repellence) should be considered with caution in integrated pest management programs.

The effect of insecticides on the non-target predatory mite Kampimodromus aberrans: laboratory studies.

The side-effects of pesticides on predatory mites have been investigated at various levels and international teams (e.g., the IOBC/wprs Working Group "Pesticides and beneficial organisms") have selected a few species of predatory mites occurring in Central and Northern Europe as representative for such studies. Key biocontrol species occurring in Southern Europe have received much less attention. Kampimodromus aberrans is the most important predator of herbivorous mites in South-European vineyards treated with selective pesticides. The impact of pesticides on K. aberrans populations has been studied in field conditions whereas few toxicological tests have been conducted in the laboratory because of difficulties in rearing this species. A method for rearing K. aberrans in the laboratory has recently been set up allowing toxicological studies to be conducted. In this paper, a toxicological method to assess the effects of pesticides on K. aberrans is described and the effects of insecticides frequently used in European vineyards on two K. aberrans strains are reported. These strains were collected from vineyards treated with organophosphates. Insecticides characterized by different modes of action were selected for trials. Among these, etofenprox and spinosad were classified as harmful to predatory mites. Chlorpyrifos reduced predatory mite fecundity, and was classified as moderately harmful for both strains. The toxicity of thiamethoxam and flufenoxuron varied with the strain (low to moderate). Indoxacarb and methoxyfenozide appeared to be harmless or slightly harmful. Implications of this study for adopting IPM tactics with a reduced risk for K. aberrans are discussed.

Resistance to acaricides in Italian strains of Tetranychus urticae: toxicological and enzymatic assays.

Problems with Tetranychus urticae are frequently reported in protected crops in Italy, particularly in roses where many introduced acaricides show a progressive loss of effectiveness. We have conducted bioassays to assess the response of some Italian strains of T. urticae to a number of acaricides. These include compounds that were widespread and frequently used in the past, but also some recently registered compounds. We investigated two T. urticae strains collected from rose growers where control failures were reported (SAN and PSE), together with a strain collected from unsprayed vegetables (BOSA). Adult females of the rose strains (SAN and PSE) were resistant to tebufenpyrad (Resistant Ratio-RR, RR(50) = 48.4 and 163.6) and fenpyroximate (RR(50) = 74.1 and 25.9) when compared to the susceptible BOSA strain. Lethal concentrations for these products were higher than the registered field rate. The PSE strain proved to be highly resistant to abamectin (RR(50) = 1,294.1). Variation in bifenazate susceptibility was detected amongst strains, but LC(90) values of SAN and PSE were still in the range of the registered field rate. In egg bioassays, the SAN and PSE strains exhibited high resistance levels to clofentezine (RR(50) = 66,473 and 170,714), hexythiazox (RR(50) = 70,244 and 159,493) and flufenoxuron (RR(50) = 61.9 and 117.9). But the recently introduced ovi/larvicides etoxazole and spirodiclofen exhibited high activity on all strains. The activity of detoxifying enzymes such as esterases, glutathione-S-transferases (GSTs) and cytochrome P450 monooxygenases (MFOs) was determined in these strains as a preliminary attempt to identify potential resistance mechanisms. Enzymatic assays showed that the rose strains exhibited 2.66 and 1.95-fold increased MFOs activity compared to the susceptible strain. Assays for GSTs revealed that only the SAN strain exhibited a significantly higher activity. In contrast, only the PSE strain showed a significant higher hydrolysis of 1-naphthyl acetate.

Resistance to chlorpyriphos in the predatory mite Kampimodromus aberrans.

The predatory mite Kampimodromus aberrans (Oudemans) is a key biocontrol agent in vineyards in Italy and Southern Europe. Its susceptibility to common pesticides (e.g., organophosphates) has been considered an important factor in preventing successful biocontrol of phytophagous mites. Nevertheless, populations of K. aberrans apparently resistant to organophosphates (OPs) have been reported to occur in Northern Italian vineyards. The resistance of K. aberrans to fungicides (e.g., mancozeb) has been demonstrated in the laboratory in France, but little is known about the toxicity of insecticides towards K. aberrans. Of these pesticides, the OP chlorpyriphos is extensively used in viticulture to control lepidopterans and homopterans. The present study investigated the dose-response effect of chlorpyriphos in four K. aberrans strains characterized by different levels of exposure to OP insecticides in the past: from never to frequently exposed. Resistance to chlorpyriphos is demonstrated for populations collected from vineyards and apple orchards. Resistance factors exceeded 145,000× for the three strains collected in vineyards and orchard. LC(50) values for resistant strains were 1.85-6.83 times higher than the recommended field dose of chlorpyriphos for vineyards and orchards (525 mg a.i./l).

Toxicity of thiamethoxam to Tetranychus urticae Koch and Phytoseiulus persimilis Athias-Henriot (Acari Tetranychidae, Phytoseiidae) through different routes of exposure.

BACKGROUND: Knowledge of the impact of insecticides on Tetranychus urticae Koch and its predator Phytoseiulus persimilis Athias-Henriot is crucial for IPM. This study evaluates the effect of thiamethoxam on T. urticae and its predator by considering different routes of exposure (topical, residual and contaminated food exposures) and their combinations. RESULTS: Thiamethoxam effects on T. urticae were higher when residual and contaminated food exposures were considered. The total effect was higher than 90% where contaminated food exposure was involved. On P. persimilis, the total effect was higher in residual and contaminated prey exposures compared with topical exposure, and all combinations of routes of exposure attained a total effect higher than 90%. CONCLUSION: Thiamethoxam was found to be toxic to T. urticae and P. persimilis; however, the impact of the insecticide depended on the routes of exposure and their combinations. Lethal and sublethal effects occurred in residual and contaminated food exposures, while only sublethal effects occurred in topical exposure of predators and prey. The toxicity of thiamethoxam on prey and predator increased with the number of exposure routes involved. By limiting exposure to thiamethoxam to ingestion of contaminated food only, the impact of the pesticide was more favourable to P. persimilis than to its prey.